Note
OCCURRENCE AND BIOLOGICAL ASPECTS OF
THE CLITORIA TREE PSYLLID IN BRAZIL
Manoel Guedes Corrêa Gondim Junior*; Reginaldo Barros; Fernando Rodrigues da Silva; Geraldo José Nascimento de Vasconcelos
UFRPE - Depto. de Agronomia/Fitossanidade, 52171-900 - Recife, PE - Brasil. *Corresponding author <[email protected]>
ABSTRACT:Clitoria fairchildiana (Howard) is a tree largely distributed in Brazil, used for urban arborization. In April 2001, the psyllidEuphalerus clitoriae Burckhardt & Guajará was reported on this plant in the metropolitan areas of Recife, PE, Brazil. This report records the occurrence of E. clitoriae and studies some of its biological aspects in this area. With this purpose, C. fairchildiana leaves were sampled weekly, and E. clitoriae nymphs as well as Aprostocetus sp. larvae and nymphs were collected and counted. The E. clitoriae population ranged from 2 to 90 nymphs per leaflet. The Aprostocetus sp. percentage of parasitism ranged from 3 to 24%. The frequency curve for pygidium width ranged from 120 to 140; 200 to 240; 300 to 380; 460 to 580, and 720 to 820 µm for the first, second, third, fourth, and fifth instars, respectively. The incubation period for E. clitoriae eggs lasted 7.6 days. The nymphal stage lasted 5.7; 4.5; 4.8; 5.0, and 6.1 days for the first, second, third, fourth, and fifth instars, respectively. Development time from egg to adult was 33.7 days. Female longevity 8.6 days, with a daily fecundity of 118 eggs. The total viability of the immature stage was 74%, and the sex ratio was 0.5.
Key words: Euphalerus clitoriae, Psyllidae, biology, biological control, natural enemies
OCORRÊNCIA E ASPECTOS BIOLÓGICOS DO
PSILÍDEO DO SOMBREIRO NO BRASIL
RESUMO: O sombreiro Clitoria fairchildiana (Howard) é uma planta amplamente distribuída no Brasil sendo muito utilizada em arborizações. Em abril de 2001 foi constatada a ocorrência do psilídeo Euphalerus clitoriae Burckhardt & Guajará neste hospedeiro na Região Metropolitana do Recife, PE. Este trabalho teve como objetivo registrar a ocorrência de E. clitoriae e seus inimigos naturais, e estudar alguns aspectos da biologia deste psilídeo. Foram realizadas coletas semanais de folhas de C. fairchildiana visando à contagem de ninfas de E. clitoriae e formas imaturas e adultos dos inimigos naturais. A população de E. clitoriae variou de 2 a 90 ninfas por folíolo. A percentagem de parasitismo de Aprostocetus sp. variou de 3 a 24%. A curva de freqüência da largura do pigídio dos insetos observados apresentou variação de 120 a 140; 200 a 240; 300 a 380; 460 a 580 e 720 a 820 µm para o primeiro, segundo, terceiro, quarto e quinto ínstares, respectivamente. Os ovos de E. clitoriae apresentaram 7,6 dias de incubação. A fase ninfal apresentou 5,7 dias para o primeiro ínstar, 4,5 dias para o segundo ínstar, 4,8 dias para o terceiro ínstar, 5,0 dias para o quarto ínstar e 6,1 dias para o quinto ínstar. O período de ovo-adulto foi 33,7 dias, a longevidade de fêmeas foi 8,6 dias e a fecundidade de 118 ovos/fêmea. A viabilidade total de formas imaturas foi de 74% e a razão sexual de 0,5.
Palavras-chave:Euphalerus clitoriae, Psyllidae, biologia, controle biológico, inimigos naturais
INTRODUCTION
The clitoria tree,Clitoria fairchildiana (Howard) (Fabaceae: Papilionoidea) is commonly used as an urban tree in several states in Brazil (Guajará et al., 2003). In the city of Recife-PE, this species is used either for ur-ban arborization of streets, squares, and gardens, or in parking lots as a shade tree. In May 1999, this species was reported as a host for the psyllid Euphalerus clitoriae
Burckhardt & Guajará, in the city of Seropédica-RJ (Burckhardt & Guajará, 2000).
Psyllids are small, soft-bodied insects, measuring 2 to 5 mm in length, resembling miniature cicadas. They have three ocelli, with well-developed and usually ten-segmented antennae, jumping hind legs in the adult, dimerous tarsal claws, and membranous wings (Borror & DeLong, 1988).
E. clitoriae preferentially colonizes the abaxial
first instar, under which the nymphs are protected (Guajará et al., 2002). This insect causes severe damage to the clitoria tree, continuously sucking young branches and leaves, which become yellow and then fall (Docile et al., 2000).
At present, several studies were conducted in or-der to clarify behavioral and biological aspects of this in-sect on C. fairchildiana in the State of Rio de Janeiro (Docile et al., 2000; Santos et al., 2000a; Guajará et al., 2002; 2003). In April 2001, the occurrence of E. clitoriae
was verified in clitoria tree plants from several localities in the cities of Recife, Olinda, Jaboatão dos Guararapes, and Cabo de Santo Agostinho, in the State of Pernambuco. This study was carried out to record the oc-currence of E. clitoriae and its natural enemies in the city of Recife onC. fairchildiana, and to study some aspects of its biology, such as duration of the immature stages, longevity, fecundity, and total viability.
MATERIAL AND METHODS
The research was performed in a laboratory un-der the following conditions: 26 ± 0.5°C, 65 ± 10% R.H., and 12h photophase. C. fairchildiana leaves were col-lected between the months of July 2001 and May 2002, in the city of Recife, PE, Brazil (08°01’02" S and 34°56’43" W). To accomplish this, ten trifoliolate leaves from the middle part of the branches of four adult plants were collected weekly. The leaves were taken to the labo-ratory and the numbers ofE. clitoriae nymphs and natu-ral enemies were tallied.
To obtain seedlings,C. fairchildiana seeds were planted in 250 mL capacity plastic cups, using a clay loam soil and earthworm humus at a 4:1 ratio as substrate. The cups were watered daily, and 15 days after planting the seedlings showed only the first pair of leaves; plants at this stage were used to rear E. clitoriae. Adults were col-lected in the field, brought to the laboratory, and confined for eight hours in cages containing 15-day old plantlets. The cages consisted of plastic tubes 10 cm in length and four centimeters in diameter. The lid was cut out and drilled in the middle to allow the plantlet stem to be in-serted through it. The base of the tube was cut out and a fine screen was glued in place to allow aeration.
Plantlets containing eggs between zero and eight hours of age were observed every 12 hours to determine the incubation period. After hatching and at every ecdysis, 20 nymphs had their pygidia measured with an ocular micrometer attached to a stereoscopic microscope to de-termine the number of instars. After hatching, the nymphs continued to be observed at 12 hours intervals to deter-mine the duration of each instar. Viability of the devel-opment stage was also determined.
After emergence, the adults were sexed in order to determine the sex ratio. Males were confined
individu-ally in cages for longevity determination. Females were confined in cages with males obtained in the field, which were replaced in case of death, and were observed daily for fecundity and longevity determination.
RESULTS AND DISCUSSION
Occurrence of E. clitoriae and its natural enemies
Nymphal ectoparasite, belonging to the family Eulophidae, subfamily Tetrastichinae, and genus
Aprostocetus were found in all sampled plants. The
hy-menopterans that belong to species in this genus fre-quently parasitize spiders and insects belonging to order Orthoptera, Lepidoptera, Coleoptera, Diptera, Hy-menoptera, and Hemiptera (Gaines & Kok, 1999; Hall et al., 2001; Mirchev et al., 2001). Among hemipterans, the species of this genus parasitize aphids, coccids, pseudococcids, and psyllids (LaSalle, 1993; Ulgenturk, 2001). This Aprostocetus species was found in the Recife metropolitan area, ectoparasitizing third-, fourth-, and fifth-instar E. clitoriae nymphs.
Mites of the families Cheyletidae and Stigmaeidae were found in laboratory, under the wax layer secreted by the nymphs. Such places are probably used as shelter by the mites, which probably also feed on sugary secretions (honeydew) produced by the psyllids. However, it was observed in the laboratory that these mites are predators on first-instar E. clitoriae nymphs, which still do not present a waxy scale. Mites of the fami-lies Cheyletidae and Stigmaeidae are predators frequently found on plants, feeding mainly on mites and occasion-ally on other small arthropods (Flechtmann, 1975).
Cheletogenes ornatus (Canestrini & Fanzago) is a
natu-ral enemy of citrus scale insects and is an important com-ponent in combination with other agents for the biologi-cal control of sbiologi-cale insects (Avidov, 1970).
Among the predators that belong to Insecta, two coccinellid species were found preying on nymphs of all instars, as well as one species of Neuroptera. These preda-tors were observed attacking E. clitoriae when the infes-tation was high, but did not remain on the plants when the population was low. Marques et al. (2002) reported the occurrence of the fungus Cladosporium
cladosporioides (Fres.) De Vries on E. clitoriae in the city
of Recife, PE. These authors verified that this pathogen infects nymphs, producing a parasitism rate of up to 12.5%.
TheE. clitoriae population ranged from
ranged from 3 to 24%, and the highest parasitism oc-curred at the beginning of the evaluation, between the months of July and September/01, decreasing to lower values when the highest host population density was veri-fied around the months of December/01 and January/02. As time went by, the E. clitoriae population increased considerably, as well as the population of Aprostocetus
sp., despite the fact that the parasitism percentage de-creased. This, in addition to the fact that Aprostocetus is not a genus frequently associated with insects in the fam-ily Psyllidae, suggests that E. clitoriae probably is not a preferential host for this parasitoid.
The E. clitoriae population increased
consider-ably from August to November 2001, when lower pre-cipitation and relative humidity prevailed, with higher temperatures, and was considerably reduced from March to July, when greater precipitation and relative humidity prevailed, with lower temperatures. Sahu & Mandal (1999) studied the seasonality ofEuphalerus vittatus on
Cassia fistula in the western part of Bengala and
veri-fied a greater occurrence of the psyllid during the months with milder temperatures and higher relative humidity.
During the period of higher E. clitoriae popula-tion density, C. fairchildiana plants presented a large number of yellow leaves and marked leaf shedding. Faeth et al. (1981); Stiling & Simberloff (1989); and Stromgren & Lanciani (2001) also verified leaf shedding in plants
Figure 1 - Population fluctuation of Euphalerus clitoriae and
Aprostocetus sp. clitoria tree (Clitoria fairchildiana), between July 2001 and January 2002.
infested with psyllids. Although leaf shedding for this species is an intrinsic trait, apparently E. clitoriae has highlighted this fact, since this is a deciduous species; this aspect has been verified by other authors as well, such as Santos et al. (2000a) and Docile et al. (2000).
E. clitoriae Biology
The psyllid adults oviposited individual eggs or laid them in clusters. The eggs were elongated, stalked, and laid preferentially on younger parts of the plant, such as shoots and young leaves, having a yellowish-green color, becoming black after a period of 24 to 48 hours. Conceição et al. (2000a) also observed the same color changing aspect in E. clitoriae eggs. The first-instar nymphs became fixed near the egg and started feeding on the leaves, secreting a small amount of wax. In the second instar, they started secreting a larger amount of wax, forming a whitish scale that entirely covered the body. This wax layer was observed in subsequent instars. Leaves with high psyllid infestations showed their abaxial surfaces completely covered with a large amount of white waxy material, secreted by the nymphs. These aspects have been reported by Guajará et al. (2002).
The pygidium in E. clitoriae was covered by a chitinous plate, which did not vary in size along each in-star. The frequency curve built from the insect pygidium width measurements showed variations from 120 to 140 (first instar), 200 to 240 (second instar), 300 to 380 (third instar), 460 to 580 (fourth instar), and 720 to 820 µm (fifth instar) (Figure 2). The growth ratios between in-stars (Table 1), varied from 1.48 to 1.54. These values agree with Dyar’s rule and can therefore be applied to insects of the family Psyllidae, using the pygidium width as a parameter.
The incubation of E. clitoriae eggs lasted 7.6 days on average; this value was close to that reported by Guajará et al. (2003) for the same host. The nymphal stages had the following durations: 5.7 days for the first instar; 4.5 days for the second instar; 4.8 days for the third instar; 5.0 days for the fourth instar; and 6.1 days for the fifth instar. The egg-adult period lasted 33.7 days, female
Figure 2 -Euphalerus clitoriae pygidium width frequency curve on clitoria tree (Clitoria fairchildiana), expressed in micrometers. Period 0 10 20 30 Psyllidae Eulophidae 0 20 40 60 80 100 0 7 14 21 28 0 20 40 60 80 100 Mean weekly precipitation (mm)
Mean weekly temperature (°C)
Mean weekly relative humidity (%)
T em per at ur e (° C ) an d P re c ipi ta ti o n (mm ) N u mb er of n y m phs /l e a fl et R e la ti v e h u m id it y (% ) Pa ra si ti sm (% ) Ju l Au g Au g Au g Se p Se p Oc t Oc t No v No v De c De c Ja n Ja n Ja n Fe b Ma r Ap r Ma y 1 Instar ↓ 2 Instar ↓ 3 Instar
↓ 4 Instar ↓ 5 Instar ↓ 0 2 4 6 8 10 12 14 16 18 20
0 40 80 120 160 200 240 280 320 360 400 440 480 520 560 600 640 680 720 760 800 840 880
F re q u e n c e
longevity was 8.6 days, and the females showed a mean fecundity of 118 eggs (Table 2). E. clitoriae has been mentioned by other authors as having an egg-adult pe-riod of 34 days, longevity of 9.17 days, and total fecun-dity of 225.29 eggs per female (Conceição et al., 2000b; Guajará et al., 2003).
Total viability of the immature forms was 74%, with a sex ratio of 0.5. Similar values were observed by Tsai & Liu (2000), who studied the biology of Diaphorina
citri under similar conditions as those verified here, and
observed a total viability ranging from 68.6 to 84.6%.
E. clitoreae is a recent pest in the Recife
Metro-politan Area and occurs at high infestations, causing se-rious damage to clitoria tree plants. This pest is partially controlled by some ectoparasitoid and predator species, and possibly by pathogens as well, and suffers the influ-ence of climatic factors. Apparently, some of these agents are nonspecific; however, with time it is likely that these natural enemies will become adapted; this, in addition to environmental factors, may keep the pest equilibrium level at lower values than at present.
ACKNOWLEDGEMENTS
To Dr. Ayres de Oliveira Menezes Júnior, from Universidade Estadual de Londrina-PR, for identifying the parasitoid Aprostocetus sp. (Hymenoptera: Eulophidae).
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Table 1 - Mean pygidium width in Euphalerus clitoriae nymphs, expressed in micrometers, and growth ratio.
Instar Pygidium Width (µm) Growth Ratio
Mean ± s(m)
I 147 ± 2 1.48
II 217 ± 3 1.55
III 337 ± 5 1.54
IV 518 ± 10 1.50
V 776 ± 6
-Table 2 - Euphalerus clitoriae development time and longevity (days), and fecundity (number of eggs per female) on butterfly pea (Clitoria fairchildiana) at 26 ± 0.5 oC, 65 ± 10% RH and 12h photophase.
Stage/Parameter No.1 Min.2 Max.3 Mean ± s(m) 4
Egg 97 7 9 7.6 ± 0.07
Nymph I 74 4.5 7 5.7 ± 0.09
Nymph II 52 3.5 6.5 4.5 ± 0.08
Nymph III 50 4 6 4.8 ± 0.09
Nymph IV 37 4 6.5 5.0 ± 0.12
Nymph V 32 5 7.5 6.1 ± 0.12
Egg-Adult 32 29 39 33.7 ± 0.47
Longevity 22 5 14 8.6 ± 0.60
Fecundity 22 47 268 117.6 ± 4.2
1Number of observations,2Minimum observed value,3Maximum
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